Ongoing shuffling of protein fragments diversifies core viral functions linked to interactions with bacterial hosts.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
28 Nov 2023
28 Nov 2023
Historique:
received:
12
06
2023
accepted:
03
11
2023
medline:
30
11
2023
pubmed:
29
11
2023
entrez:
28
11
2023
Statut:
epublish
Résumé
Biological modularity enhances evolutionary adaptability. This principle is vividly exemplified by bacterial viruses (phages), which display extensive genomic modularity. Phage genomes are composed of independent functional modules that evolve separately and recombine in various configurations. While genomic modularity in phages has been extensively studied, less attention has been paid to protein modularity-proteins consisting of distinct building blocks that can evolve and recombine, enhancing functional and genetic diversity. Here, we use a set of 133,574 representative phage proteins and highly sensitive homology detection to capture instances of domain mosaicism, defined as fragment sharing between two otherwise unrelated proteins, and to understand its relationship with functional diversity in phage genomes. We discover that unrelated proteins from diverse functional classes frequently share homologous domains. This phenomenon is particularly pronounced within receptor-binding proteins, endolysins, and DNA polymerases. We also identify multiple instances of recent diversification via domain shuffling in receptor-binding proteins, neck passage structures, endolysins and some members of the core replication machinery, often transcending distant taxonomic and ecological boundaries. Our findings suggest that ongoing diversification via domain shuffling is reflective of a co-evolutionary arms race, driven by the need to overcome various bacterial resistance mechanisms against phages.
Identifiants
pubmed: 38016962
doi: 10.1038/s41467-023-43236-9
pii: 10.1038/s41467-023-43236-9
pmc: PMC10684548
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
7460Subventions
Organisme : Narodowe Centrum Nauki (National Science Centre)
ID : 2020/37/B/NZ8/03492
Organisme : Narodowe Centrum Nauki (National Science Centre)
ID : 2020/37/B/NZ8/03492
Organisme : Narodowe Centrum Nauki (National Science Centre)
ID : 2020/37/B/NZ8/03492
Organisme : Fundacja na rzecz Nauki Polskiej (Foundation for Polish Science)
ID : POIR.04.04.00-00-5CF1/18-00
Informations de copyright
© 2023. The Author(s).
Références
Artif Life. 2007 Summer;13(3):249-58
pubmed: 17567244
Proc Natl Acad Sci U S A. 2010 Aug 10;107(32):14384-9
pubmed: 20660769
BMC Struct Biol. 2003 Jan 28;3:1
pubmed: 12553882
Nucleic Acids Res. 2002 Apr 1;30(7):1575-84
pubmed: 11917018
Nat Microbiol. 2022 Jul;7(7):1028-1040
pubmed: 35725776
Proteins. 1994 Dec;20(4):347-55
pubmed: 7731953
Cell. 2023 Apr 27;186(9):1863-1876.e16
pubmed: 37030292
Arch Virol. 2023 Jun 10;168(7):175
pubmed: 37296227
Bioinformatics. 2005 Apr 1;21(7):951-60
pubmed: 15531603
PLoS Biol. 2022 Jan 13;20(1):e3001514
pubmed: 35025885
Analyst. 2020 Sep 28;145(19):6291-6297
pubmed: 32945826
Nat Rev Microbiol. 2018 Dec;16(12):760-773
pubmed: 30104690
J R Soc Interface. 2018 Dec 21;15(149):20180595
pubmed: 30958230
J Mol Biol. 2018 Jul 20;430(15):2237-2243
pubmed: 29258817
Proc Natl Acad Sci U S A. 2021 Apr 20;118(16):
pubmed: 33846247
BMC Bioinformatics. 2019 Sep 14;20(1):473
pubmed: 31521110
Nat Commun. 2023 Jul 20;14(1):4336
pubmed: 37474554
Nature. 2003 May 8;423(6936):139-44
pubmed: 12736677
Nat Biotechnol. 2017 Nov;35(11):1026-1028
pubmed: 29035372
Nature. 1976 Jun 17;261(5561):552-8
pubmed: 934293
Curr Opin Struct Biol. 2008 Jun;18(3):358-65
pubmed: 18457946
Evolution. 2002 Aug;56(8):1549-56
pubmed: 12353747
Nat Rev Microbiol. 2013 Oct;11(10):675-87
pubmed: 23979432
Curr Opin Biotechnol. 2021 Apr;68:272-281
pubmed: 33744824
NAR Genom Bioinform. 2021 Aug 05;3(3):lqab067
pubmed: 34377978
BMC Biol. 2020 Jun 9;18(1):61
pubmed: 32517760
Microbiol Mol Biol Rev. 2011 Sep;75(3):423-33, first page of table of contents
pubmed: 21885679
Viruses. 2019 Jul 09;11(7):
pubmed: 31324000
Sci Adv. 2020 Jun 03;6(23):eaaz1136
pubmed: 32537492
mBio. 2021 May 4;12(3):
pubmed: 33947754
Protein Sci. 2022 Jul;31(7):e4362
pubmed: 35762715
Mol Biol Evol. 2008 Apr;25(4):762-77
pubmed: 18234706
Trends Microbiol. 2019 Jan;27(1):51-63
pubmed: 30181062
Genome Inform. 2009 Oct;23(1):205-11
pubmed: 20180275
Front Microbiol. 2018 May 18;9:1033
pubmed: 29867909
PLoS Biol. 2022 Aug 1;20(8):e3001740
pubmed: 35913996
Cell. 2018 Mar 8;172(6):1260-1270
pubmed: 29522746
J Mol Biol. 2006 Aug 4;361(1):46-68
pubmed: 16828113
J Mol Biol. 2006 Jun 2;359(2):496-507
pubmed: 16631788
Science. 2018 Mar 2;359(6379):
pubmed: 29371424
Adv Exp Med Biol. 2019;1148:233-253
pubmed: 31482502
Nat Rev Microbiol. 2020 Feb;18(2):113-119
pubmed: 31695182
Curr Opin Virol. 2022 Feb;52:182-191
pubmed: 34952266
Science. 2023 Jan 13;379(6628):195-201
pubmed: 36634164
Nucleic Acids Res. 2016 Jun 2;44(10):4551-64
pubmed: 27112572
Viruses. 2021 Jun 26;13(7):
pubmed: 34206969
ISME J. 2020 Jul;14(7):1713-1730
pubmed: 32249276
J Mol Biol. 2004 Oct 8;343(1):1-28
pubmed: 15381417
Protein Sci. 2018 Aug;27(8):1450-1463
pubmed: 29722076
Bioinformatics. 2023 Oct 3;39(10):
pubmed: 37725369
Nucleic Acids Res. 2017 Jan 4;45(D1):D170-D176
pubmed: 27899574
PeerJ. 2021 May 6;9:e11396
pubmed: 33996289
Nucleic Acids Res. 2014 Apr;42(7):4160-79
pubmed: 24464998
mBio. 2016 Aug 02;7(4):
pubmed: 27486193
G3 (Bethesda). 2021 May 7;11(5):
pubmed: 33734357
Nat Rev Genet. 2007 Dec;8(12):921-31
pubmed: 18007649
Curr Opin Virol. 2011 Oct;1(4):298-303
pubmed: 22034588
Sci Rep. 2016 Feb 19;6:21345
pubmed: 26892066
Evolution. 1996 Jun;50(3):967-976
pubmed: 28565291
Cell Rep. 2019 Oct 29;29(5):1336-1350.e4
pubmed: 31665644
Nat Commun. 2022 Nov 24;13(1):7241
pubmed: 36433970
Proc Natl Acad Sci U S A. 2005 Sep 27;102(39):13773-8
pubmed: 16174729
Genome Biol Evol. 2014 Aug 07;6(9):2195-205
pubmed: 25104113
FEMS Microbiol Rev. 2022 Feb 9;46(1):
pubmed: 34558600
Cell. 2022 Oct 13;185(21):4023-4037.e18
pubmed: 36174579
Nature. 1999 Dec 2;402(6761 Suppl):C47-52
pubmed: 10591225
Nat Rev Microbiol. 2020 Mar;18(3):125-138
pubmed: 32015529
Res Microbiol. 2011 Oct;162(8):737-46
pubmed: 21767638
J Biol Chem. 1995 Nov 3;270(44):26558-64
pubmed: 7592876
Prog Biophys Mol Biol. 2018 Jan;132:43-51
pubmed: 28801037
Sci Rep. 2020 Jan 15;10(1):307
pubmed: 31941920
Nat Methods. 2011 Dec 25;9(2):173-5
pubmed: 22198341
Philos Trans R Soc Lond B Biol Sci. 2006 Mar 29;361(1467):507-17
pubmed: 16524839
Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
pubmed: 9254694
Int J Mol Sci. 2022 Jan 07;23(2):
pubmed: 35054821
Curr Gene Ther. 2017;17(2):120-126
pubmed: 28494733
Sci Rep. 2021 Jan 25;11(1):2164
pubmed: 33495501
FEMS Microbiol Rev. 2005 Apr;29(2):231-62
pubmed: 15808743
PLoS Comput Biol. 2014 Dec 04;10(12):e1003926
pubmed: 25474468
Cell Host Microbe. 2022 Apr 13;30(4):570-582.e7
pubmed: 35421352
Bioinformatics. 2021 Aug 25;37(16):2473-2475
pubmed: 33459763
Nat Rev Microbiol. 2020 Jun;18(6):344-359
pubmed: 32055025
Mol Biol Evol. 2021 May 19;38(6):2497-2512
pubmed: 33570565
PLoS One. 2012;7(3):e34052
pubmed: 22470512
Mol Microbiol. 2014 Mar;91(5):862-74
pubmed: 24405365
Nat Rev Genet. 2020 Dec;21(12):754-768
pubmed: 32860017
Front Microbiol. 2019 Nov 15;10:2649
pubmed: 31803168
J Mol Evol. 2002 Jun;54(6):763-73
pubmed: 12029358
Proc Natl Acad Sci U S A. 1999 Mar 2;96(5):2192-7
pubmed: 10051617
Genome Biol Evol. 2011;3:456-75
pubmed: 21602570
Nat Commun. 2022 May 10;13(1):2561
pubmed: 35538097
Cell Host Microbe. 2017 Dec 13;22(6):801-808.e3
pubmed: 29174401
Nat Biotechnol. 2019 Jun;37(6):632-639
pubmed: 31061483
Ann N Y Acad Sci. 1980;354:484-90
pubmed: 6452848
Nature. 1992 Jun 18;357(6379):543-4
pubmed: 1608464
Mol Biol Evol. 2021 May 19;38(6):2191-2208
pubmed: 33502503